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Concomitant duplications of opioid peptide and receptor genes before the origin of jawed vertebrates.

Sundström G, Dreborg S, Larhammar D - PLoS ONE (2010)

Bottom Line: The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings.However, subsequently genetic linkage has been lost.In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The opioid system is involved in reward and pain mechanisms and consists in mammals of four receptors and several peptides. The peptides are derived from four prepropeptide genes, PENK, PDYN, PNOC and POMC, encoding enkephalins, dynorphins, orphanin/nociceptin and beta-endorphin, respectively. Previously we have described how two rounds of genome doubling (2R) before the origin of jawed vertebrates formed the receptor family.

Methodology/principal findings: Opioid peptide gene family members were investigated using a combination of sequence-based phylogeny and chromosomal locations of the peptide genes in various vertebrates. Several adjacent gene families were investigated similarly. The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings. The fourth member was generated by a local gene duplication, as the genes encoding POMC and PNOC are located on the same chromosome in the chicken genome and all three teleost genomes that we have studied. A translocation has disrupted this synteny in mammals. The PDYN gene seems to have been lost in chicken, but not in zebra finch. Duplicates of some peptide genes have arisen in the teleost fishes. Within the prepropeptide precursors, peptides have been lost or gained in different lineages.

Conclusions/significance: The ancestral peptide and receptor genes were located on the same chromosome and were thus duplicated concomitantly. However, subsequently genetic linkage has been lost. In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

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Neighbor-Joining tree for the opioid prepropeptide family.Bootstrap values are shown at the nodes. Abbreviations: PENK preproenkephalin, PDYN preprodynorphin, PNOC preproorphanin and POMC proopioimelanocortin.
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pone-0010512-g001: Neighbor-Joining tree for the opioid prepropeptide family.Bootstrap values are shown at the nodes. Abbreviations: PENK preproenkephalin, PDYN preprodynorphin, PNOC preproorphanin and POMC proopioimelanocortin.

Mentions: Opioid peptide precursor genes were identified in the genome databases for human, mouse, dog, grey short-tailed opossum, chicken, western clawed frog, zebrafish, medaka and stickleback, accession numbers for all sequences are available in Table S1. It was not possible to identify peptide genes in any of the basal chordate genomes we studied, Ciona intestinalis and Branchiostoma floridae and therefore the phylogenetic tree is displayed unrooted, see Fig. 1. The POMC gene in lampreys has been duplicated early in their evolution generating the precursor genes named POC and POM [24]. We have not included POC and POM protein sequences in our study since their evolution has been thoroughly studied by others and no other opioid precursor sequences have been reported for lampreys and thus they will not shed light on the origin of the four members in gnathostomes. For some vertebrates it was possible to identify the opioid peptide sequences using BLAST searches in their genomes. However, in a few cases only incomplete sequences were found, but also these sequences clustered in the phylogenetic tree together with their orthologues in other species. One such example is PDYN from zebra finch. The stem of the POMC cluster is longer than for the other three genes as a result of the insertion of the melanocortin sequences into this precursor, see Fig. 1.


Concomitant duplications of opioid peptide and receptor genes before the origin of jawed vertebrates.

Sundström G, Dreborg S, Larhammar D - PLoS ONE (2010)

Neighbor-Joining tree for the opioid prepropeptide family.Bootstrap values are shown at the nodes. Abbreviations: PENK preproenkephalin, PDYN preprodynorphin, PNOC preproorphanin and POMC proopioimelanocortin.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2865548&req=5

pone-0010512-g001: Neighbor-Joining tree for the opioid prepropeptide family.Bootstrap values are shown at the nodes. Abbreviations: PENK preproenkephalin, PDYN preprodynorphin, PNOC preproorphanin and POMC proopioimelanocortin.
Mentions: Opioid peptide precursor genes were identified in the genome databases for human, mouse, dog, grey short-tailed opossum, chicken, western clawed frog, zebrafish, medaka and stickleback, accession numbers for all sequences are available in Table S1. It was not possible to identify peptide genes in any of the basal chordate genomes we studied, Ciona intestinalis and Branchiostoma floridae and therefore the phylogenetic tree is displayed unrooted, see Fig. 1. The POMC gene in lampreys has been duplicated early in their evolution generating the precursor genes named POC and POM [24]. We have not included POC and POM protein sequences in our study since their evolution has been thoroughly studied by others and no other opioid precursor sequences have been reported for lampreys and thus they will not shed light on the origin of the four members in gnathostomes. For some vertebrates it was possible to identify the opioid peptide sequences using BLAST searches in their genomes. However, in a few cases only incomplete sequences were found, but also these sequences clustered in the phylogenetic tree together with their orthologues in other species. One such example is PDYN from zebra finch. The stem of the POMC cluster is longer than for the other three genes as a result of the insertion of the melanocortin sequences into this precursor, see Fig. 1.

Bottom Line: The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings.However, subsequently genetic linkage has been lost.In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The opioid system is involved in reward and pain mechanisms and consists in mammals of four receptors and several peptides. The peptides are derived from four prepropeptide genes, PENK, PDYN, PNOC and POMC, encoding enkephalins, dynorphins, orphanin/nociceptin and beta-endorphin, respectively. Previously we have described how two rounds of genome doubling (2R) before the origin of jawed vertebrates formed the receptor family.

Methodology/principal findings: Opioid peptide gene family members were investigated using a combination of sequence-based phylogeny and chromosomal locations of the peptide genes in various vertebrates. Several adjacent gene families were investigated similarly. The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings. The fourth member was generated by a local gene duplication, as the genes encoding POMC and PNOC are located on the same chromosome in the chicken genome and all three teleost genomes that we have studied. A translocation has disrupted this synteny in mammals. The PDYN gene seems to have been lost in chicken, but not in zebra finch. Duplicates of some peptide genes have arisen in the teleost fishes. Within the prepropeptide precursors, peptides have been lost or gained in different lineages.

Conclusions/significance: The ancestral peptide and receptor genes were located on the same chromosome and were thus duplicated concomitantly. However, subsequently genetic linkage has been lost. In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

Show MeSH